Lung hyperpermeability and asthma prevalence in schoolchildren: unexpected associations with the attendance at indoor chlorinated swimming pools
Open accessAbstract
Aims:To study whether exposure to nitrogen trichloride in indoor chlorinated pools may affect the respiratory epithelium of children and increase the risk of some lung diseases such as asthma. Methods:In 226 healthy children, serum surfactant associated proteins A and B (SP-A and SP-B), 16 kDa Clara cell protein (CC16), and IgE were measured. Lung specific proteins were measured in the serum of 16 children and 13 adults before and after exposure to NCl 3 in an indoor chlorinated pool. Relations between pool attendance and asthma prevalence were studied in 1881 children. Asthma was screened with the exercise induced bronchoconstriction test (EIB). Results:Pool attendance was the most consistent predictor of lung epithelium permeability. A positive dose-effect relation was found with cumulated pool attendance and serum SP-A and SP-B. Serum IgE was unrelated to pool attendance, but correlated positively with lung hyperpermeability as assessed by serum SP-B. Changes in serum levels of lung proteins were reproduced in children and adults attending an indoor pool. Serum SP-A and SP-B were already significantly increased after one hour on the pool side without swimming. Positive EIB and total asthma prevalence were significantly correlated with cumulated pool attendance indices. Conclusions:Regular attendance at chlorinated pools by young children is associated with an exposure dependent increase in lung epithelium permeability and increase in the risk of developing asthma, especially in association with other risk factors. We therefore postulate that the increasing exposure of children to chlorination products in indoor pools might be an important cause of the rising incidence of childhood asthma and allergic diseases in industrialised countries. Further epidemiological studies should be undertaken to test this hypothesis.
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Chloramine levels have been associated with ceiling height and free chlorine concentration in the water.
“Chloramine levels have been associated with ceiling height and free chlorine concentration in the water 7, 14.”
From Exposure to trichloramine and respiratory symptoms in indoor swimming pool workers (2007) · cites this paper as [7]
The Discussion (page unavailable) uses pool-hall height as a surrogate for air quality and says chlorine dosing affects the composition of air above the water. It does not report an association between measured chloramine levels and ceiling height or free-chlorine concentration in the water. (LLM, conf=0.78)
Experimental — accuracy not yet measuredOther studies have reported that exposure to irritants can cause irritation and inflammatory effects on the airways.
“Other studies have reported that exposure to irritants can cause irritation and inflammatory effects on the airways 7, 18–20.”
From Exposure to trichloramine and respiratory symptoms in indoor swimming pool workers (2007) · cites this paper as [7]
The introduction (page unavailable) describes nitrogen trichloride as an irritant associated with upper-respiratory-tract irritation. The Discussion (page unavailable) reports lung-epithelial permeability changes from chlorination products and compares them with changes occurring during inflammation, but does not establish that the exposure caused airway inflammation. (LLM, conf=0.82)
Experimental — accuracy not yet measuredOne of the main culprits for the pool-related effects could be trichloramine, which damages swimmers' lung epithelium and causes occupational asthma in lifeguards.
“One of the main culprits could be trichloramine, the gas that gives indoor pools their characteristic chlorine smell and that has recently been found to damage the lung epithelium of swimmers (Bernard et al. 2003; Carbonnelle et al. 2002; Lagerkvist et al. 2004) and to cause occupational asthma in lifeguards (Thickett et al. 2002).”
From Chlorinated Pool Attendance, Atopy, and the Risk of Asthma during Childhood (2006) · cites this paper as Bernard et al. 2003
The Discussion reports evidence that exposure to chlorination products in indoor pools may harm swimmers’ lung epithelium and identifies nitrogen trichloride as a prominent airborne oxidant. The Acute effects section measured epithelial changes after pool exposure, but the study did not isolate trichloramine as the cause. The lifeguard asthma claim is attributed to Thickett et al., not Bernard et al. (LLM, conf=0.85)
Experimental — accuracy not yet measuredAir measurements of trichloramine during competitive and recreational swimming were similar to those measured during pool work, i.e. 0.2-1.30 mg/m3.
“Exposure levels during swimming were similar to those measured during pool work, i.e. 0.2-1.30mg/m 3”
From Inorganic chloramines: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting (2020) · cites this paper as Bernard et al. 2003
The Acute effects section (page not supplied) reports a mean nitrogen trichloride concentration of 0.490 mg/m³ during a pool experiment involving swimmers. The Discussion (page not supplied) gives public-pool air ranges of 0.1–1 and 0.14–0.8 mg/m³. Neither passage reports the claimed 0.2–1.30 mg/m³ range or compares competitive and recreational swimming with pool work. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThe information on exposure assessments of trichloramine in the three Belgian studies is very sparse, making it difficult to relate exposure to reported effects.
“The information on the exposure assessments of trichloramine in these three Belgian studies (Bernard et al. 2003(Bernard et al. , 2006(Bernard et al. , 2009) is very sparse regarding sampling time, where measurements were performed and number of samples.This makes it difficult to relate the exposure of trichloramine to the effects reported.”
From Inorganic chloramines: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting (2020) · cites this paper as Bernard et al. 2003
The Study of acute effects section says trichloramine was measured at 1.5 m, and the Acute effects results give a mean concentration, but neither passage specifies the sampling schedule or number of samples. The Discussion also reports measurements in eight Brussels pools. This supports the concern about limited detail in the 2003 paper, though the paper does give some measurement-location information and cannot establish what the other two Belgian studies reported. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Effects on pneumoproteins were shown at trichloramine concentrations ≥0.29 mg/m3, but not at lower exposure levels.
“Effects on pneumoproteins were shown at trichloramine concentrations !0.29 mg/m 3 (Carbonnelle et al. 2002;Bernard et al. 2003;Font-Ribera et al. 2010), but not at lower exposure levels (Carbonnelle et al. 2008;Nordberg et al. 2012).”
From Inorganic chloramines: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting (2020) · cites this paper as Bernard et al. 2003
The ‘Acute effects on the lung epithelium’ section reports significant increases in serum SP-A and SP-B during exposure at a mean trichloramine concentration of 0.490 mg/m³. That supports an effect at a concentration above 0.29 mg/m³, but the paper does not establish 0.29 mg/m³ as a threshold. The lower-exposure clause cites other papers, not Bernard et al. (LLM, conf=0.83)
Experimental — accuracy not yet measuredAsthma risk is increased only in children with elevated serum IgE, whereas inflammatory effects associated with pool attendance seem to concern all pool attendees.
“Thus, whereas asthma risk was increased only in children with elevated serum IgE, inflammatory effects associated with pool attendance, such as the effects on the pulmonary epithelium (Bernard et al. 2003; Carbonnelle et al. 2002; Lagerkvist et al. 2004), seem to concern all pool attendees.”
From Chlorinated Pool Attendance, Atopy, and the Risk of Asthma during Childhood (2006) · cites this paper as Bernard et al. 2003
Transient changes in serum pneumoproteins associated with changes in lung epithelium permeability were seen in some studies at airborne trichloramine concentrations ≥0.3 mg/m3, whereas no such effects were observed in studies at lower mean exposure levels.
“Transient changes in serum pneumoproteins associated with changes in lung epithelium permeability were seen in some studies at airborne trichloramine concentrations !0.3 mg/m 3 (Carbonnelle et al. 2002;Bernard et al. 2003;Font-Ribera et al. 2010), whereas no such effects were observed in studies at lower mean exposure levels (Carbonnelle et al. 2008;Nordberg et al. 2012).”
From Inorganic chloramines: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting (2020) · cites this paper as Bernard et al. 2003
In a cross-sectional study of Belgian children, prevalence of respiratory symptoms was not associated with positive EIB test or total asthma (positive EIB test and/or medication for asthma).
“Prevalence of respiratory symptoms was not associated | with positive EIB test or total asthma (positive EIB | test and/or medication for asthma).”
From Inorganic chloramines: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting (2020) · cites this paper as Bernard et al. (2003)
In that study, positive EIB test and total asthma prevalence were significantly associated with cumulative pool attendance.
“Positive EIB test | and total asthma prevalence were significantly | associated with cumulative pool attendance.”
From Inorganic chloramines: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting (2020) · cites this paper as Bernard et al. (2003)
In that study, the associations remained significant after adjustment for pool height, pets and passive smoking, and were strongest among the youngest children (p < 0.001).
“The | associations remained significant after adjustment | for pool height, pets and passive smoking, and were | strongest among the youngest children (p < 0.001)”
From Inorganic chloramines: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting (2020) · cites this paper as Bernard et al. (2003)
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Wastensson, G., & Eriksson, K. (2020) · Critical Reviews in Toxicology · doi:10.1080/10408444.2020.1744514 · Cited by 30 · see citing works
Font-Ribera, L., Villanueva, C. M., Gràcia-Lavedan, E., Borràs-Santos, A., Kogevinas, M., & Zock, J.-P. (2014) · Respiratory Medicine · doi:10.1016/j.rmed.2014.04.018 · Cited by 28 · see citing works
Chlorine, Chlorination By-Products and Their Allergic and Respiratory Health Effects
Kohlhammer, Y., & Heinrich, J. (2007) · Current Respiratory Medicine Reviews · doi:10.2174/157339807779941839 · Cited by 13 · see citing works
Training does not affect exhaled nitric oxide in competitive swimmers
Moreira, A., Delgado, L., Haahtela, T., Silva, J. A., Araújo, L., Beça, F., Fonseca, J., & Castel‐Branco, M. G. (2008) · Allergy · doi:10.1111/j.1398-9995.2008.01659.x · Cited by 10 · see citing works
- Authors
- Bernard, A., Carbonnelle, S., Michel, O., Higuet, S., de Burbure, C., Buchet, J.-P., Hermans, C., Dumont, X., & Doyle, I.
- Affiliations
- UCLouvain (BE)
- Centre Hospitalier Universitaire de Saint-Pierre (BE)
- Flinders University (AU)
- Corresponding author
- Bernard, A
- Venue
- Occupational and Environmental Medicine
- Publisher
- BMJ
- Published
- 2003-06
- Volume
- 60
- Issue
- 6
- Pages
- 385-394
- ISSN
- 0007-1072 (ISSN-L)
- 1351-0711
- 1470-7926
- PMC
- PMC1740550
- OpenAlex
- W2168585771
- Cited by
- 256
- References
- 44
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 1 · 2023: 4 · 2022: 3 · 2021: 6 · 2020: 9 · 2019: 7 · 2018: 9 · 2017: 6 · 2016: 8 · 2015: 15 · 2014: 15 · 2013: 14 · 2012: 16
- FWCI
- 6.90
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Occupational and Environmental Medicine (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DIAL (Catholic University of Leuven) (submittedVersion, other-oa)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
- Funders
- AstraZeneca
- Université Catholique de Louvain
- European Commission
- Flinders University
- Ministry of Environment
- Vrije Universiteit Brussel
- Topics
- Health Sciences › Medicine › Physiology › Asthma and respiratory diseases
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Occupational exposure and asthma
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Indoor Air Quality and Microbial Exposure
- Keywords
- nitrogen trichloride, asthma, childhood asthma, lung epithelial permeability, surfactant-associated proteins, surfactant protein A, surfactant protein B, Clara cell secretory protein, IgE, exercise-induced bronchoconstriction, elementary school students, chlorine exposure, allergic diseases
- MeSH terms
- Adolescent, Asthma, Child, Child, Preschool, Chlorides, Dose-Response Relationship, Drug, Exercise Test, Humans, Immunoglobulin E, Lung, Permeability, Proteins, Swimming Pools, Uteroglobin, Bronchoconstriction, Nitrogen Compounds, Respiratory Mucosa, Pulmonary Surfactant-Associated Protein A, Pulmonary Surfactant-Associated Protein B
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